Somatotopic organization among parallel sensory pathways that promote a grooming sequence in Drosophila

Eichler, Katharina; Hampel, Stefanie; Alejandro-García, Adrián; Calle-Schuler, Steven A; Santana-Cruz, Alexis; Kmecova, Lucia; Blagburn, Jonathan M; Hoopfer, Eric D; Seeds, Andrew M

doi:10.7554/elife.87602.3

Cited by 5Neurobiology and Insect Physiology ResearchNeuroscience and Neuropharmacology ResearchTactile and Sensory Interactions

Somatotopic organization among parallel sensory pathways that promote a grooming sequence in Drosophila

Open access

Eichler, Katharina, Hampel, Stefanie, Alejandro-García, Adrián, Calle-Schuler, Steven A, Santana-Cruz, Alexis, Kmecova, Lucia, Blagburn, Jonathan M, Hoopfer, Eric D +1 more·2024·eLife

DOI 10.7554/elife.87602.3

Published version of a preprint

Open this paper in CoChat — free account

Abstract

Mechanosensory neurons located across the body surface respond to tactile stimuli and elicit diverse behavioral responses, from relatively simple stimulus location-aimed movements to complex movement sequences. How mechanosensory neurons and their postsynaptic circuits influence such diverse behaviors remains unclear. We previously discovered that Drosophila perform a body location-prioritized grooming sequence when mechanosensory neurons at different locations on the head and body are simultaneously stimulated by dust (Hampel et al., 2017; Seeds et al., 2014). Here, we identify nearly all mechanosensory neurons on the Drosophila head that individually elicit aimed grooming of specific head locations, while collectively eliciting a whole head grooming sequence. Different tracing methods were used to reconstruct the projections of these neurons from different locations on the head to their distinct arborizations in the brain. This provides the first synaptic resolution somatotopic map of a head, and defines the parallel-projecting mechanosensory pathways that elicit head grooming.

Integrity signals

Registry

Crossref · 10.7554/elife.87602.3

Cites

113 of 113 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Schlegel et al. and other community members were able to determine the sensory organs corresponding to the 5,375 non-visual sensory neurons on the basis of morphology and nerve assignments.
“Although afferents are truncated in our reconstruction, Schlegel et al.12 and other community members35,57 were able to determine the sensory organs corresponding to the 5,375 non-visual sensory neurons (Fig. 2e,f) on the basis of morphology and nerve assignments.”
From Neuronal wiring diagram of an adult brain (2024) · cites this paper as [35]
FlyWire community members have shared 133,700 annotations of 114,209 neurons, including comprehensive cell typing in the optic lobe, the majority of sexually dimorphic neurons and sensory neurons, and a diversity of cell types throughout the brain, including the SEZ.
“FlyWire community members, many of whom are experts in diverse regions of the fly brain, have shared 133,700 annotations of 114,209 neurons (Supplementary Fig. 9), including comprehensive cell typing in the optic lobe11, the majority of sexually dimorphic neurons and sensory neurons35, as well as a diversity of cell types throughout the brain, including the SEZ (Fig. 2f).”
From Neuronal wiring diagram of an adult brain (2024) · cites this paper as [35]

Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
Cytoscape: A software Environment for integrated models of biomolecular interaction networks
Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., & Ideker, T. (2003) · Genome Research · doi:10.1101/gr.1239303 · Cited by 51,888 · see citing works
Independent optical excitation of distinct neural populations
Klapoetke, N. C., Murata, Y., Kim, S. S., Pulver, S. R., Birdsey-Benson, A., Cho, Y. K., Morimoto, T. K., Chuong, A. S., Carpenter, E. J., Tian, Z., et al. (2014) · Nature Methods · doi:10.1038/nmeth.2836 · Cited by 2,344 · see citing works
The Sensory Neurons of Touch
Abraira, V. E., & Ginty, D. D. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.051 · Cited by 1,648 · see citing works
A GAL4-Driver Line Resource for Drosophila Neurobiology
Jenett, A., Rubin, G. M., Ngo, T.-T. B., Shepherd, D., Murphy, C., Dionne, H., Pfeiffer, B. D., Cavallaro, A., Hall, D., Jeter, J., et al. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.09.011 · Cited by 1,449 · see citing works
Refinement of Tools for Targeted Gene Expression in Drosophila
Pfeiffer, B. D., Ngo, T.-T. B., Hibbard, K. L., Murphy, C., Jenett, A., Truman, J. W., & Rubin, G. M. (2010) · Genetics · doi:10.1534/genetics.110.119917 · Cited by 1,153 · see citing works
A Complete Electron Microscopy Volume of the Brain of Adult Drosophila melanogaster
Zheng, Z., Lauritzen, J. S., Perlman, E., Robinson, C. G., Nichols, M., Milkie, D., Torrens, O., Price, J., Fisher, C. B., Sharifi, N., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.019 · Cited by 1,050 · see citing works
Self-citation
Development of the Drosophila retina, a neurocrystalline lattice
Ready, D. F., Hanson, T. E., & Benzer, S. (1976) · Developmental Biology · doi:10.1016/0012-1606(76)90225-6 · Cited by 1,030 · see citing works
Tools for neuroanatomy and neurogenetics in Drosophila
Pfeiffer, B. D., Jenett, A., Hammonds, A. S., Ngo, T.-T. B., Misra, S., Murphy, C., Scully, A. L., Carlson, J. W., Wan, K. H., Laverty, T., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803697105 · Cited by 974 · see citing works
The organization of the chemosensory system in Drosophila melanogaster: a rewiew
Stocker, R. F. (1994) · Cell and Tissue Research · doi:10.1007/bf00305372 · Cited by 950 · see citing works
Cerebral mechanisms in behavior.
indicated, N. A. (1952) · Journal of Consulting Psychology · doi:10.1037/h0051344 · Cited by 918 · see citing works
A Drosophila Mechanosensory Transduction Channel
Walker, R. G., Willingham, A. T., & Zuker, C. S. (2000) · Science · doi:10.1126/science.287.5461.2229 · Cited by 696 · see citing works
Comprehensive Maps of Drosophila Higher Olfactory Centers: Spatially Segregated Fruit and Pheromone Representation
Jefferis, G. S. X. E., Potter, C. J., Chan, A. M., Marin, E. C., Torsten Rohlfing, B., Maurer, C. R., & Luo, L. (2007) · Cell · doi:10.1016/j.cell.2007.01.040 · Cited by 647 · see citing works
Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system
Nern, A., Pfeiffer, B. D., & Rubin, G. M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1506763112 · Cited by 584 · see citing works
Refined Spatial Manipulation of Neuronal Function by Combinatorial Restriction of Transgene Expression
Luan, H., Peabody, N. C., Vinson, C. R., & White, B. H. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.028 · Cited by 500 · see citing works
Topographic Maps are Fundamental to Sensory Processing
Kaas, J. H. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00094-4 · Cited by 478 · see citing works
The neural basis of Drosophila gravity-sensing and hearing
Kamikouchi, A., Inagaki, H. K., Effertz, T., Hendrich, O., Fiala, A., Göpfert, M. C., & Ito, K. (2009) · Nature · doi:10.1038/nature07810 · Cited by 406 · see citing works
Neural representations and mechanisms for the performance of simple speech sequences
Bohland, J. W., Bullock, D., & Guenther, F. H. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21306 · Cited by 393 · see citing works
Structure and Function of the Deutocerebrum in Insects
Homberg, U., Christensen, T. A., & Hildebrand, J. G. (1989) · Annual Review of Entomology · doi:10.1146/annurev.en.34.010189.002401 · Cited by 353 · see citing works
NBLAST: Rapid, Sensitive Comparison of Neuronal Structure and Construction of Neuron Family Databases
Costa, M., Manton, J. D., Ostrovsky, A. D., Prohaska, S., & Jefferis, G. S. X. E. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.012 · Cited by 294 · see citing works
neuTube 1.0: A New Design for Efficient Neuron Reconstruction Software Based on the SWC Format
Feng, L., Zhao, T., & Kim, J. (2015) · eNeuro · doi:10.1523/eneuro.0049-14.2014 · Cited by 292 · see citing works
Mechanosensation and Adaptive Motor Control in Insects
Tuthill, J. C., & Wilson, R. I. (2016) · Current Biology · doi:10.1016/j.cub.2016.06.070 · Cited by 290 · see citing works
FlyWire: online community for whole-brain connectomics
Dorkenwald, S., McKellar, C. E., Macrina, T., Kemnitz, N., Lee, K., Lu, R., Wu, J., Popovych, S., Mitchell, E., Nehoran, B., et al. (2022) · Nature Methods · doi:10.1038/s41592-021-01330-0 · Cited by 289 · see citing works
Parallel processing of serial movements in prefrontal cortex
Averbeck, B. B., Chafee, M. V., Crowe, D. A., & Georgopoulos, A. P. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.162485599 · Cited by 287 · see citing works
Distinct sensory representations of wind and near-field sound in the Drosophila brain
Yorozu, S., Wong, A. M., Fischer, B. J., Dankert, H., Kernan, M. J., Kamikouchi, A., Ito, K., & Anderson, D. J. (2009) · Nature · doi:10.1038/nature07843 · Cited by 268 · see citing works
Reconstruction of motor control circuits in adult drosophila using automated transmission electron microscopy
Phelps, J. S., Hildebrand, D. G. C., Graham, B. J., Kuan, A. T., Thomas, L. A., Nguyen, T. M., Buhmann, J., Azevedo, A. W., Sustar, A., Agrawal, S., et al. (2021) · Cell · doi:10.1016/j.cell.2020.12.013 · Cited by 265 · see citing works
The morphology of hair follicle afferent fibre collaterals in the spinal cord of the cat
Brown, A. G., Rose, P. K., & Snow, P. J. (1977) · The Journal of Physiology · doi:10.1113/jphysiol.1977.sp012073 · Cited by 249 · see citing works
Activity in the lateral prefrontal cortex reflects multiple steps of future events in action plans
Mushiake, H., Saito, N., Sakamoto, K., Itoyama, Y., & Tanji, J. (2006) · Neuron · doi:10.1016/j.neuron.2006.03.045 · Cited by 249 · see citing works
Genetic Reagents for Making Split-GAL4 Lines in Drosophila
Dionne, H., Hibbard, K. L., Cavallaro, A., Kao, J.-C., & Rubin, G. M. (2018) · Genetics · doi:10.1534/genetics.118.300682 · Cited by 232 · see citing works
Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster
Kamikouchi, A., Shimada, T., & Ito, K. (2006) · Journal of Comparative Neurology · doi:10.1002/cne.21075 · Cited by 220 · see citing works
Drosophila cholinergic neurons and processes visualized with Gal4/UAS–GFP
Salvaterra, P. M., & Kitamoto, T. (2001) · Gene Expression Patterns · doi:10.1016/s1567-133x(01)00011-4 · Cited by 219 · see citing works
Drosophila Brainbow: a recombinase-based fluorescence labeling technique to subdivide neural expression patterns
Hampel, S., Chung, P., McKellar, C. E., Hall, D., Looger, L. L., & Simpson, J. H. (2011) · Nature Methods · doi:10.1038/nmeth.1566 · Cited by 219 · see citing works
Self-citation
The VT GAL4, LexA, and split-GAL4 driver line collections for targeted expression in the Drosophila nervous systemPreprint
Tirián, L., & Dickson, B. J. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/198648 · Cited by 217 · see citing works
The natverse, a versatile toolbox for combining and analysing neuroanatomical data
Bates, A. S., Manton, J. D., Jagannathan, S. R., Costa, M., Schlegel, P., Rohlfing, T., & Jefferis, G. S. (2020) · eLife · doi:10.7554/elife.53350 · Cited by 215 · see citing works
The Molecular Diversity of Dscam Is Functionally Required for Neuronal Wiring Specificity in Drosophila
Chen, B. E., Kondo, M., Garnier, A., Watson, F. L., Püettmann-Holgado, R., Lamar, D. R., & Schmucker, D. (2006) · Cell · doi:10.1016/j.cell.2006.03.034 · Cited by 209 · see citing works
Sensilla on the tarsal segments and mouthparts of adult Drosophila melanogaster meigen (Diptera : Drosophilidae)
Nayak, S. V., & Singh, R. (1983) · International Journal of Insect Morphology and Embryology · doi:10.1016/0020-7322(83)90023-5 · Cited by 205 · see citing works
A suppression hierarchy among competing motor programs drives sequential grooming in Drosophila
Seeds, A. M., Ravbar, P., Chung, P., Hampel, S., Midgley, F. M., Mensh, B. D., & Simpson, J. H. (2014) · eLife · doi:10.7554/elife.02951 · Cited by 200 · see citing works
Self-citation
Gustatory organs of Drosophila melanogaster : fine structure and expression of the putative odorant-binding protein PBPRP2
Shanbhag, S. R., S.-K., P., Pikielny, C. W., & Steinbrecht, R. A. (2001) · Cell and Tissue Research · doi:10.1007/s004410100388 · Cited by 185 · see citing works
A neural command circuit for grooming movement control
Hampel, S., Franconville, R., Simpson, J. H., & Seeds, A. M. (2015) · eLife · doi:10.7554/elife.08758 · Cited by 177 · see citing works
Self-citation
Automatic detection of synaptic partners in a whole-brain Drosophila electron microscopy data set
Buhmann, J., Sheridan, A., Malin-Mayor, C., Schlegel, P., Gerhard, S., Kazimiers, T., Krause, R., Nguyen, T. M., Heinrich, L., Lee, W.-C. A., et al. (2021) · Nature Methods · doi:10.1038/s41592-021-01183-7 · Cited by 175 · see citing works
Localization of nicotinic receptor subunit mRNAs in monkey brain by in situ hybridization
Quik, M., Polonskaya, Y., Gillespie, A. J., Jakowec, M. W., Lloyd, G. K., & Langston, J. W. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20000911)425:1 · Cited by 172 · see citing works
Optogenetic dissection of descending behavioral control in Drosophila
Cande, J., Namiki, S., Qiu, J., Korff, W., Card, G. M., Shaevitz, J. W., Stern, D. L., & Berman, G. J. (2018) · eLife · doi:10.7554/elife.34275 · Cited by 163 · see citing works
The topographic brain: from neural connectivity to cognition
Thivierge, J., & Marcus, G. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.04.004 · Cited by 158 · see citing works
Distinct Roles of TRP Channels in Auditory Transduction and Amplification in Drosophila
Lehnert, B. P., Baker, A. E., Gaudry, Q., Chiang, A., & Wilson, R. I. (2013) · Neuron · doi:10.1016/j.neuron.2012.11.030 · Cited by 157 · see citing works
Neuronal wiring diagram of an adult brain
Dorkenwald, S., Matsliah, A., Sterling, A. R., Schlegel, P., Yu, S.-C., McKellar, C. E., Lin, A., Costa, M., Eichler, K., Yin, Y., et al. (2023) · doi:10.1101/2023.06.27.546656 · Cited by 149 · see citing works
Self-citation
Labellar taste organs of Drosophila melanogaster
Falk, R., Bleiser‐Avivi, N., & Atidia, J. (1976) · Journal of Morphology · doi:10.1002/jmor.1051500206 · Cited by 144 · see citing works
The Basis of Food Texture Sensation in Drosophila
Zhang, Y. V., Aikin, T. J., Li, Z., & Montell, C. (2016) · Neuron · doi:10.1016/j.neuron.2016.07.013 · Cited by 134 · see citing works
Peripheral and central structures involved in insect gustation
Mitchell, B. K., Itagaki, H., & Rivet, M.-P. (1999) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(19991215)47:6 · Cited by 133 · see citing works
Fine structure and primary sensory projections of sensilla on the maxillary palp of Drosophila melanogaster Meigen (Diptera : Drosophilidae)
Singh, R., & Nayak, S. V. (1985) · International Journal of Insect Morphology and Embryology · doi:10.1016/0020-7322(85)90044-3 · Cited by 124 · see citing works
The projection of sensory neurons in the central nervous system of Drosophila: Choice of the appropriate pathway
Ghysen, A. (1980) · Developmental Biology · doi:10.1016/0012-1606(80)90351-6 · Cited by 119 · see citing works
VCode and VData
Hagedorn, J., Hailpern, J. M., & Karahalios, K. G. (2008) · Working Conference on Advanced Visual Interfaces (AVI) · doi:10.1145/1385569.1385622 · Cited by 119 · see citing works
FluoRender: An application of 2D image space methods for 3D and 4D confocal microscopy data visualization in neurobiology research
Wan, Y., Otsuna, H., Chien, C.-B., & Hansen, C. D. (2012) · IEEE Pacific Visualization Symposium · doi:10.1109/pacificvis.2012.6183592 · Cited by 118 · see citing works
Cobalt filling of sensory projections from internal and external mouthparts in Drosophila
Stocker, R. F., & Schorderet, M. (1981) · Cell and Tissue Research · doi:10.1007/bf00238648 · Cited by 118 · see citing works
Adaptive neural models of queuing and timing in fluent action
Bullock, D. H. (2004) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.07.003 · Cited by 117 · see citing works
Synaptic Cleft Segmentation in Non-isotropic Volume Electron Microscopy of the Complete Drosophila Brain
Heinrich, L., Funke, J., Pape, C., Nunez-Iglesias, J., & Saalfeld, S. (2018) · Lecture Notes in Computer Science · doi:10.1007/978-3-030-00934-2_36 · Cited by 117 · see citing works
Genetic control of sensory connections in Drosophila
Vandervorst, P., & Ghysen, A. (1980) · Nature · doi:10.1038/286065a0 · Cited by 116 · see citing works
Modality‐specific axonal projections in the CNS of the flies Phormia and Drosophila
Murphey, R. K., Possidente, D. R., Pollack, G. S., & Merritt, D. J. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902900203 · Cited by 116 · see citing works
A mechanosensory receptor required for food texture detection in Drosophila
Sánchez‐Alcañiz, J. A., Zappia, G., Marion‐Poll, F., & Benton, R. (2017) · Nature Communications · doi:10.1038/ncomms14192 · Cited by 116 · see citing works
Neurotransmitter Classification from Electron Microscopy Images at Synaptic Sites in Drosophila Melanogaster
Eckstein, N., Bates, A. S., Champion, A., Du, M., Yin, Y., Schlegel, P., Lu, A. K.-Y., Rymer, T., Finley-May, S., Paterson, T., et al. (2020) · doi:10.1101/2020.06.12.148775 · Cited by 115 · see citing works
Self-citation
Topological and modality-specific representation of somatosensory information in the fly brain
Tsubouchi, A., Yano, T., Yokoyama, T. K., Murtin, C., Otsuna, H., & Ito, K. (2017) · Science · doi:10.1126/science.aan4428 · Cited by 108 · see citing works
Whisker-Mediated Touch System in Rodents: From Neuron to Behavior
Adibi, M. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2019.00040 · Cited by 106 · see citing works
Mechanosensory neurons control sweet sensing in Drosophila
Jeong, Y. T., Oh, S. M., Shim, J., Seo, J. T., Kwon, J. Y., & Moon, S. J. (2016) · Nature Communications · doi:10.1038/ncomms12872 · Cited by 100 · see citing works
Projections of leg proprioceptors within the CNS of the fly Phormia in relation to the generalized insect ganglion
Merritt, D. J., & Murphey, R. K. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903220103 · Cited by 99 · see citing works
Genetic depletion of histamine from the nervous system of Drosophila eliminates specific visual and mechanosensory behavior
Melzig, J., Buchner, S., Wiebel, F. F., Wolf, R., Buchner, E., Burg, M. G., & Pak, W. L. (1996) · Journal of Comparative Physiology A · doi:10.1007/bf00207355 · Cited by 99 · see citing works
Habituation and dishabituation of a cleaning reflex in normal and mutant Drosophila
Corfas, G., & Dudai, Y. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-01-00056.1989 · Cited by 99 · see citing works
Encoding of Wind Direction by Central Neurons in Drosophila
Suver, M. P., Matheson, A. M. M., Sarkar, S., Damiata, M., Schoppik, D., & Nagel, K. I. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.012 · Cited by 99 · see citing works
Parallel Transformation of Tactile Signals in Central Circuits of Drosophila
Tuthill, J. C., & Wilson, R. I. (2016) · Cell · doi:10.1016/j.cell.2016.01.014 · Cited by 97 · see citing works
Isolation of mutations affecting neural circuitry required for grooming behavior in Drosophila melanogaster.
Phillis, R. W., Bramlage, A. T., Wotus, C., Whittaker, A. J., Gramates, L. S., Seppala, D., Farahanchi, F., Caruccio, P., & Murphey, R. K. (1993) · Genetics · doi:10.1093/genetics/133.3.581 · Cited by 94 · see citing works
Hierachical organization and postural facilitation: Rules for grooming in flies
Richard, R., & Dawkins, M. S. (1976) · Animal Behaviour · doi:10.1016/s0003-3472(76)80003-6 · Cited by 92 · see citing works
Functional Maps of Mechanosensory Features in the Drosophila Brain
Patella, P., & Wilson, R. I. (2018) · Current Biology · doi:10.1016/j.cub.2018.02.074 · Cited by 92 · see citing works
The afferent projection of mesothoracic bristle hairs in the cricket,Acheta domesticus
Johnson, S. E., & Murphey, R. K. (1985) · Journal of Comparative Physiology A · doi:10.1007/bf00610729 · Cited by 88 · see citing works
Cleaning behaviour in Drosophila melanogaster
Szebenyi, A. L. (1969) · Animal Behaviour · doi:10.1016/s0003-3472(69)80006-0 · Cited by 87 · see citing works
Morphology and somatotopic organisation of the central projections of afferents from tactile hairs on the hind leg of the locust
Newland, P. L. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903120402 · Cited by 87 · see citing works
Active and Passive Antennal Movements during Visually Guided Steering in FlyingDrosophila
Mamiya, A., Straw, A. D., Tómasson, E., & Dickinson, M. H. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0498-11.2011 · Cited by 85 · see citing works
Neural Representations of Courtship Song in theDrosophilaBrain
Tootoonian, S., Coen, P., Kawai, R., & Murthy, M. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5104-11.2012 · Cited by 84 · see citing works
Neural architecture of the primary gustatory center of Drosophila melanogaster visualized with GAL4 and LexA enhancer‐trap systems
Miyazaki, T., & Ito, K. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22433 · Cited by 83 · see citing works
Sensory projections from the wind-sensitive head hairs of the locust Schistocerca gregaria
Tyrer, N. M., Bacon, J. P., & Davies, C. A. (1979) · Cell and Tissue Research · doi:10.1007/bf00234330 · Cited by 83 · see citing works
Neural pathways for the detection and discrimination of conspecific song in D. melanogaster
Vaughan, A. G., Zhou, C., Manoli, D. S., & Baker, B. S. (2014) · Current Biology · doi:10.1016/j.cub.2014.03.048 · Cited by 81 · see citing works
Adaptation and fatigue of a mechanosensory neuron in wild-type Drosophila and in memory mutants
Corfas, G., & Dudai, Y. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-02-00491.1990 · Cited by 70 · see citing works
Compartments and the topography of leg afferent projections in Drosophila
Murphey, R. K., Possidente, D. R., Vandervorst, P., & Ghysen, A. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-09-03209.1989 · Cited by 70 · see citing works
Simultaneous activation of parallel sensory pathways promotes a grooming sequence in Drosophila
Hampel, S., McKellar, C. E., Simpson, J. H., & Seeds, A. M. (2017) · eLife · doi:10.7554/elife.28804 · Cited by 70 · see citing works
Self-citation
Identification of novel vibration- and deflection-sensitive neuronal subgroups in Johnston's organ of the fruit fly
Matsuo, E., Yamada, D., Ishikawa, Y., Asai, T., Ishimoto, H., & Kamikouchi, A. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00179 · Cited by 65 · see citing works
A Defensive Kicking Behavior in Response to Mechanical Stimuli Mediated byDrosophilaWing Margin Bristles
Li, J., Zhang, W., Guo, Z., Wu, S., Jan, L. Y., & Jan, Y. N. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1416-16.2016 · Cited by 65 · see citing works
Descending neurons coordinate anterior grooming behavior in Drosophila
Guo, L., Zhang, N., & Simpson, J. H. (2022) · Current Biology · doi:10.1016/j.cub.2021.12.055 · Cited by 63 · see citing works
Central Generation of Grooming Motor Patterns and Interlimb Coordination in Locusts
Berkowitz, A., & Laurent, G. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-24-08079.1996 · Cited by 62 · see citing works
The Function of Hair Sensilla on the Locust’s Leg: the Role Of tibial hairs
Pflüger, H. (1980) · Journal of Experimental Biology · doi:10.1242/jeb.87.1.163 · Cited by 61 · see citing works
Neural control of leg movements in a metamorphic insect: Sensory and motor elements of the larval thoracic legs in Manduca sexta
Kent, K. S., & Levine, R. B. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902710407 · Cited by 59 · see citing works
Connectomics and the neural basis of behaviour
Galili, D. S., Jefferis, G. S. X. E., & Costa, M. (2022) · Current Opinion in Insect Science · doi:10.1016/j.cois.2022.100968 · Cited by 59 · see citing works
Drosophila melanogaster grooming possesses syntax with distinct rules at different temporal scales
Mueller, J. M., Ravbar, P., Simpson, J. H., & Carlson, J. M. (2019) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1007105 · Cited by 54 · see citing works
Hindleg Targeting During Scratching in the Locust
Matheson, T. (1997) · Journal of Experimental Biology · doi:10.1242/jeb.200.1.93 · Cited by 52 · see citing works
Spatial Comparisons of Mechanosensory Information Govern the Grooming Sequence in Drosophila
Zhang, N., Guo, L., & Simpson, J. H. (2020) · Current Biology · doi:10.1016/j.cub.2020.01.045 · Cited by 50 · see citing works
Mechanosensory circuits coordinate two opposing motor actions in Drosophila feeding
Zhou, Y., Cao, L.-H., Sui, X.-W., Guo, X.-Q., & Luo, D.-G. (2019) · Science Advances · doi:10.1126/sciadv.aaw5141 · Cited by 49 · see citing works
Wing hair sensilla underlying aimed hindleg scratching of the locust
Page, K., & Matheson, T. (2004) · Journal of Experimental Biology · doi:10.1242/jeb.01096 · Cited by 46 · see citing works
Antennal Mechanosensory Neurons Mediate Wing Motor Reflexes in FlyingDrosophila
Mamiya, A., & Dickinson, M. H. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0034-15.2015 · Cited by 44 · see citing works
Interommatidial hair receptor axons extending into the ventral nerve cord in the cricket Gryllus campestris
Honegger, H. (1977) · Cell and Tissue Research · doi:10.1007/bf00220597 · Cited by 43 · see citing works
Neurotransmitter regulation of circadian structural changes in the fly's visual system
Meinertzhagen, I. A., & Pyza, E. (1999) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(19990415)45:2 · Cited by 42 · see citing works
Processing of tactile information in neuronal networks controlling leg movements of the Locust
Newland, P. L., & Burrows, M. (1997) · Journal of Insect Physiology · doi:10.1016/s0022-1910(96)00081-9 · Cited by 39 · see citing works
Drosophila gustatory projections are segregated by taste modality and connectivity
Engert, S., Sterne, G. R., Bock, D. D., & Scott, K. (2022) · eLife · doi:10.7554/elife.78110 · Cited by 38 · see citing works
Sensory mechanisms of eye cleaning behavior in the cricket Gryllus campestris
Honegger, H., Reif, H., & Müller, W. A. (1979) · Journal of Comparative Physiology A · doi:10.1007/bf00657661 · Cited by 37 · see citing works
A neural circuit integrates pharyngeal sensation to control feeding
Yang, T., Yuan, Z., Liu, C., Liu, T., & Zhang, W. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109983 · Cited by 35 · see citing works
Distinct subpopulations of mechanosensory chordotonal organ neurons elicit grooming of the fruit fly antennae
Hampel, S., Eichler, K., Yamada, D., Bock, D. D., Kamikouchi, A., & Seeds, A. M. (2020) · eLife · doi:10.7554/elife.59976 · Cited by 35 · see citing works
Self-citation
Anatomic and Physiologic Heterogeneity of Subgroup-A Auditory Sensory Neurons in Fruit Flies
Ishikawa, Y., Okamoto, N., Nakamura, M., Kim, H., & Kamikouchi, A. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00046 · Cited by 33 · see citing works
Differentiation and central projections of peripheral sensory cells with action-potential block in Drosophila mosaics
Burg, M., & Wu, C. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-10-02968.1986 · Cited by 32 · see citing works
Structural and functional analysis of single neurons to correlate synaptic connectivity with grooming behavior
Kays, I., Cvetkovska, V., & Chen, B. E. (2013) · Nature Protocols · doi:10.1038/nprot.2013.157 · Cited by 31 · see citing works
Mechanoreceptive bristles on the head of the blowfly: Mechanics and electrophysiology of the macrochaetae
Thei�, J. (1979) · Journal of Comparative Physiology A · doi:10.1007/bf00617732 · Cited by 30 · see citing works
Wiring patterns from auditory sensory neurons to the escape and song-relay pathways in fruit flies
Kim, H., Horigome, M., Ishikawa, Y., Li, F., Lauritzen, J. S., Card, G., Bock, D. D., & Kamikouchi, A. (2020) · Journal of Comparative Neurology · doi:10.1002/cne.24877 · Cited by 27 · see citing works
Central projections of peripheral mechanosensory cells with increased excitability in Drosophila mosaics
Burg, M. G., & Wu, C. (1989) · Developmental Biology · doi:10.1016/s0012-1606(89)80021-1 · Cited by 25 · see citing works
Development and maintenance of a simple reflex circuit in small‐patch mosaics of Drosophila: Effects of altered neuronal function and developmental arrest
Burg, M. G., Hanna, L., Kim, Y.-T., & Wu, C. (1993) · Journal of Neurobiology · doi:10.1002/neu.480240608 · Cited by 23 · see citing works
Peripheral Axonal Pathway and Cleaning Behavior Are Correlated in Drosophila Microchaetes
Usui-Ishihara, A., Ghysen, A., & Kimura, K. (1995) · Developmental Biology · doi:10.1006/dbio.1995.1034 · Cited by 19 · see citing works
Interommatidial sensilla of the praying mantis: Their central neural projections and role in head‐cleaning behavior
Zack, S., & Bacon, J. (1981) · Journal of Neurobiology · doi:10.1002/neu.480120105 · Cited by 18 · see citing works
THE TERMINOLOGY OF BRISTLES ON THE UPPER BACK OF THE HEAD IN THE HIGHER DIPTERA
Steyskal, G. C. (2016) · Cited by 12 · see citing works
Convergence of distinct subpopulations of mechanosensory neurons onto a neural circuit that elicits groomingPreprint
Hampel, S., Eichler, K., Yamada, D., Kim, H., Horigome, M., Franconville, R., Bock, D. D., Kamikouchi, A., & Seeds, A. M. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.08.141341 · Cited by 11 · see citing works
Self-citation
Untitled work
Zahm (1996) · doi:10.1002/(sici)1096-9861(19960108)364:2

Flagged first, then by citations

1 of the 114 references couldn’t be matched to a known paper.

Sorted by citations

Neuronal wiring diagram of an adult brain
Dorkenwald, S., Matsliah, A., Sterling, A. R., Schlegel, P., Yu, S.-C., McKellar, C. E., Lin, A., Costa, M., Eichler, K., Yin, Y., et al. (2024) · Nature · doi:10.1038/s41586-024-07558-y · Cited by 570 · see citing works
Self-citation
Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster
Eckstein, N., Bates, A. S., Champion, A., Du, M., Yin, Y., Schlegel, P., Lu, A. K.-Y., Rymer, T., Finley-May, S., Paterson, T., et al. (2024) · Cell · doi:10.1016/j.cell.2024.03.016 · Cited by 233 · see citing works
Self-citation
Mechanosensory Control of Locomotion in Animals and Robots: Moving Forward
Dallmann, C. J., Dickerson, B. H., Simpson, J. H., Wyart, C., & Jayaram, K. (2023) · Integrative and Comparative Biology · doi:10.1093/icb/icad057 · Cited by 12 · see citing works
From Sensory Detection to Motor Action: The Comprehensive Drosophila Taste-Feeding ConnectomePreprint
Tastekin, I., Vicente, I. D. H., Beresford, R. J., Morris, B. J., Beckett, I. R., Schlegel, P., Gkantia, M., FlyEM Project Team, Cambridge Connectomics Group, Marin, E. C., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.25.671814 · Cited by 3 · see citing works
Connectomes: a re-emerging hub dataset for neuroscience
Kyllmann, S., & Keesey, I. W. (2026) · Frontiers in Neuroscience · doi:10.3389/fnins.2026.1911198 · Cited by 1 · see citing works

A comprehensive mechanosensory connectome reveals a somatotopically organized neural circuit architecture controlling stimulus-aimed grooming of the Drosophila head
Calle-Schuler, S. A., Santana-Cruz, A., Kmecová, L., Hampel, S., & Seeds, A. M. (2026) · eLife · doi:10.7554/elife.108044.3 · Cited by 4 · see citing works
Self-citation
Spatial Comparisons of Mechanosensory Information Govern the Grooming Sequence in Drosophila
Zhang, N., Guo, L., & Simpson, J. H. (2020) · Current Biology · doi:10.1016/j.cub.2020.01.045 · Cited by 50 · see citing works
Mechanosensory and command contributions to the Drosophila grooming sequence
Yoshikawa, S., Tang, P., & Simpson, J. H. (2024) · Current Biology · doi:10.1016/j.cub.2024.04.003 · Cited by 13 · see citing works
Sensory inputs to Drosophila sequential grooming
Zhang, N. (2021) · eScholarship (California Digital Library)
A central somatotopic map of the fly leg supports spatially targeted grooming
Elabbady, L., Chou, G. M., Sustar, A., Cook, A., Collman, F., & Tuthill, J. C. (2026) · Current Biology · doi:10.1016/j.cub.2026.03.045 · Cited by 1 · see citing works

Authors: Eichler, K., Hampel, S., Alejandro-García, A., Calle-Schuler, S. A., Santana-Cruz, A., Kmecova, L., Blagburn, J. M., Hoopfer, E. D., & Seeds, A. M.
Affiliations: University of Puerto Rico, Medical Sciences Campus (PR)
Institute of Neurobiology, University of Puerto Rico-Medical Sciences Campus
Carleton College (US)
ORCID: Eichler, Katharina
Hampel, Stefanie
Calle-Schuler, Steven A
Santana-Cruz, Alexis
Blagburn, Jonathan M
Hoopfer, Eric D
Seeds, Andrew M
Venue: eLife
Publisher: eLife Sciences Publications, Ltd
Published: 2024-04-18
Volume: 12
ISSN: 2050-084X (ISSN-L)
DOI: 10.7554/elife.87602.3
OpenAlex: W4394931604
Cited by: 5
References: 114
Citations by year: 2026: 1 · 2025: 1 · 2024: 2 · 2023: 1
FWCI: 0.70
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
creativecommons.org/licenses/by/4.0/ (am)
creativecommons.org/licenses/by/4.0/ (tdm)
Locations: eLife (publishedVersion, cc-by)
Funders: BRAIN Initiative (1RF1NS121911-01)
Puerto Rico Science, Technology and Research Trust (2020-00195)
Whitehall Foundation (2017-12-69)
National Institute on Minority Health and Health Disparities (MD007600)
National Institute of General Medical Sciences (R25GM061838, 5R25GM061151, GM103642)
National Science Foundation (HRD-1736019)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
Keywords: somatotopic map, mechanosensory neurons, grooming, Drosophila, parallel sensory pathways, arborization, tactile stimuli, body location

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Somatotopic organization among parallel sensory pathways that promote a grooming sequence in Drosophila

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks